evidence-based practices to promote exclusive feeding of human milk in vlbw infants

DOI: 10.1542/neo.8-11-e467 2007;8;e467-e477 NeoReviews

Paula P. Meier and Janet L. Engstrom Low-birthweight Infants

Evidence-based Practices to Promote Exclusive Feeding of Human Milk in Very

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Evidence-based Practices toPromote Exclusive Feedingof Human Milk in VeryLow-birthweight InfantsPaula P. Meier, RN,DNSc,* Janet L.Engstrom, RN, PhD,CNM†

Author Disclosure

Drs Meier and

Engstrom disclosed

partial research

funding from Medela,

Inc, McHenry, Ill.

Objectives After completing this article, readers should be able to:

1. Review best practices to protect maternal milk volume in pump-dependent women.2. Describe the use of milk volume diaries in the neonatal intensive care unit.3. List common reasons for insufficient milk volume in pump-dependent women.4. Describe the roles of galactagogues and sleep and antianxiety medications in the treat-

ment of insufficient maternal milk volume.5. Explain appropriate use of the creamatocrit technique to estimate the lipid and calorie

content of human milk.

AbstractRecent studies suggest a dose-response relationship between the amount of fortifiedhuman milk (FHM) received by very low-birthweight and extremely low-birthweightinfants and protection from select prematurity-specific morbidities. However, thefeeding of high doses of FHM in this population often is precluded by insufficientmaternal milk volume and the replacement of FHM feedings with calorie-dense infantformulas to achieve adequate weight gain. This article reviews the evidence forpreventing, diagnosing, and treating insufficient maternal milk volume and slowinfant weight gain while receiving FHM and highlights the utility of incorporatingtechnologies from human milk science, such as maternal milk volume records and thecreamatocrit procedure, into routine neonatal intensive care unit practice.

IntroductionRecent studies have suggested a dose-response relationship between the amount offortified human milk (FHM) received by very low-birthweight (VLBW) (�1,500 g) andextremely low-birthweight (ELBW) (� 1,000 g) infants and protection from prematurity-specific morbidities. (1)(2)(3)(4) Although most neonatal clinicians agree that theseinfants should receive as much FHM as possible during the neonatal intensive care unit(NICU) stay, two clinical realities often make this goal unachievable. First, most mothersof pump-dependent VLBW and ELBW infants do not provide an adequate volume of milkto permit exclusive FHM feedings. (1)(2)(4)(5)(6)(7)(8) Second, such infants may notgain weight adequately on FHM when they are smallest and feeding volumes are restricted,necessitating the replacement of FHM with calorie-dense commercial formulas. (2)(9)Application of human milk research principles and technologies in the NICU can helpprevent and treat these common scenarios, allowing infants to receive a greater total doseof FHM.

Preventing and Treating Insufficient Maternal Milk VolumeNICU clinicians often perceive “running out of milk” as inevitable for mothers who deliverprematurely and focus on reassuring these women about the value of the milk they are ableto provide. Although mothers who deliver VLBW and ELBW infants are at risk for delayed

*Director for Clinical Research and Lactation, Neonatal Intensive Care Unit, Rush University Medical Center, Chicago, Ill.†Professor and Chair of Women’s and Children’s Health Nursing, Rush University Medical Center, Chicago, Ill.

Article nutrition

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lactogenesis, stress-mediated lactation problems, andother conditions that can affect milk volume adversely,preterm birth per se does not mean that women mustexperience insufficient milk volume. (6)(7)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20) However, inmany NICUs, the prevention, diagnosis, and treatmentof insufficient milk volume is not given a high priority,especially with respect to the application of evidence-based management strategies. Thus, it is probable thanmany episodes of insufficient milk volume could be pre-vented or treated if the appropriate resources were in-vested in achieving this objective.

The Prevalence of Low Milk Volume forMothers of VLBW and ELBW InfantsSeveral previous studies have documented that mothersof preterm infants experience delays in the initiation oflactation and produce less milk than their term counter-parts. (5)(6)(7)(15) In a recent study, Schanler andassociates (1) demonstrated significantly fewer episodesof late-onset sepsis or necrotizing enterocolitis and ashorter duration of hospital stay for extremely preterminfants who received exclusive FHM rather than partialFHM feedings. However, of the 187 mothers (of 243infants) in the study, only 27% were able to provideexclusive FHM for the entire NICU stay. Two secondaryanalyses from the National Institute of Child Health andHuman Development (NICHD) Neonatal Networkrandomized trial of glutamine supplementation revealedthat of the 1,057 ELBW infants in the sample, 75%received some FHM. (4)(8) However, the median vol-ume of FHM feedings for this cohort was only 30 mL/kgper day, and it appears that none of the infants receivedexclusive FHM, defined as at least 150 mL/kg per day.(4) These studies suggest that most women cannot ini-tiate and maintain a sufficient milk volume for VLBWand ELBW infants.

In contrast, in a recent two-phase randomized trialevaluating the effectiveness, efficiency, comfort, and con-venience of a hospital-grade breast pump, only 29% ofmothers of VLBW infants were unable to achieve aminimum daily milk volume at least 350 mL/d over thefirst postnatal month, which was a prerequisite for enter-ing the randomized phase of the study. (11)(12) Amongthe 35 mothers who met this criterion, the mean dailymilk volume was 639 mL, the mean number of pumpingswas 5.3, and the women pumped an average of98.4 min/d. (11)(12) Because the objective of the studywas to compare the effect of different suction patterns inan electric breast pump, all extraneous variables knownto affect maternal milk volume were controlled or mea-

sured. These evidence-based practices, equipment, andeducational principles are listed in the Table and com-prise the state of the evidence with respect to best prac-tices for protecting maternal milk volume in pump-dependent women. The application of the best practicesin the breast pump randomized trial may explain thedifferences in the prevalence of insufficient maternal milkvolume between this research and other cited studies.

Preventing Low Milk Volume: Importance ofthe First Two Postnatal WeeksA primary reason that mothers of VLBW and ELBWinfants get off to a poor start with lactation is that they donot receive appropriate information and equipment dur-ing the first 2 weeks after birth, which is a critical periodfor the initiation and maintenance of lactation.(10)(16)(21) Clinicians fear that providing numericalmilk volume targets and emphasizing the necessity offrequent (up to eight times daily) milk expression with ahospital-grade electric breast pump will make mothersanxious, so the women do not know how their milkvolumes should increase as lactogenesis progresses.Compounding this problem is that NICU personnelseldom monitor daily milk volumes for women, notingonly whether there is enough milk in the freezer for theinfant. The mismatch between the volume of milk amother needs to produce to protect lactation and thevolume required by a small infant during the first weeksafter birth sets the stage for subsequent insufficient ma-ternal milk volume.

For example, a 700-g infant needs only 105 mL ofFHM daily to receive 150 mL/kg, so the NICU staffbelieves the mother is lactating successfully if she pro-vides this volume of milk each day. However, a motherwho has such a low daily milk volume at the end of thesecond or third postnatal week is at significant risk forinsufficient milk volume later in the NICU stay. (7)(10)This situation is compounded by mothers having heardor read that “supply equals demand” with respect to milkvolume and assuming that as their infants’ feeding re-quirements increase, they will naturally make more milk.However, the mother of a VLBW or ELBW infant ispump-dependent, meaning that her milk volume is de-termined completely by the effectiveness and frequencyof breast pump use. Thus, the NICU staff must assumean active role in educating mothers about the principlesof lactogenesis for pump-dependent women and ensurethat the women have milk volume targets as well asappropriate equipment and guidelines for breast pumpuse. This process is facilitated by the use of maternal milkvolume diaries or records.

nutrition breastfeeding in preterm infants

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Table. Best Practices to Prevent, Diagnose, and Treat Insufficient MilkVolume in Pump-dependent Mothers of VLBW and ELBW InfantsPrevention

1. Provide equipment, supplies, information, and educational materials during mother’s hospital stay.Equipment and Supplies:

• Hospital-grade electric breast pump and collection kit for NICU and in-home use• Custom-fitted breast shields (sizes 24, 27, 30, 36 mm)• 11-mL colostrum storage containers• 60-mL milk storage containers• My Mom Pumps for Me! milk volume record

Information:• Physiology of lactogenesis, including milk volume targets for first 2 postnatal weeks• Discussion of identified maternal risk factors for lactation, including delayed lactogenesis II• Avoidance of hormonal birth control during early postnatal period• Guidelines for use of the hospital-grade pump• Demonstration of correct labeling, handling, storage, and transport of milk storage containers• Sharing of NICU lactation specialist telephone and pager numbers that can be accessed 24 hours a day, 7 days a

weekEducational Materials:

• Welcome to the Rush Mothers’ Milk Club folder, which includes 10 tear sheets in English and Spanish addressingcommon concerns, such as maternal diet and medications, expressing and labeling colostrum, and caring forbreast pump equipment

2. Provide nonpharmacologic interventions in the NICU that optimize maternal milk volume during the infant’shospitalization.• 24-hour visitation and access to infant• Consistent message about the importance of human milk from all NICU clinicians• Use of breast pump at infant’s bedside• Daily skin-to-skin holding in the NICU• Daily “tasting” of milk (suckling at emptied breast) after extubation, regardless of infant weight and gestation• Peer support for pumping and other NICU-specific activities with Rush Mothers’ Milk Club breastfeeding peer

counselors• Attendance at weekly Mothers’ Milk Club luncheons• Review of maternal milk volume records at least twice weekly to identify pumping patterns and detect potential

problems• Observations of mother using pump in the NICU at least once weekly to detect problems that may compromise milk

volume, including correctly fitted breast shields (size may change over time) and complete breast emptying

Diagnosis

1. Review My Mom Pumps for Me! milk volume records for 7 days prior to the onset of low milk volume to identifyprecipitating factors.

2. Observe a complete pumping session to ensure appropriate technique, equipment, and supplies.3. Review with the mother the most common reasons for low milk volume:

• Milk stasis, especially change in type of breast pump, tightly fitted breast shields, longer intervals betweenpumping, and not emptying breasts thoroughly

• New medications, especially the start of hormonal birth control methods• More intense stress, anxiety, or insomnia related to infant’s changing condition or other personal issues

Treatment

1. If insufficient milk volume is due to milk stasis, correct the underlying problem, eg, type of breast pump andequipment, frequency of breast pump use.

2. Ensure that all above nonpharmacologic interventions are being implemented.3. Determine whether the mother would be likely to respond to metoclopramide augmentation of insufficient milk

volume, and if so, organize a prescription with the mother’s primary care provider:• Primary problem should be one that would respond to increased baseline prolactin concentrations, such as

temporary milk stasis due to an ineffective breast pump(continued)




Although maternal milk volume diaries are common-place in lactation research, in which documentation ofdaily pumping frequencies, minutes, and volumes arevariables of interest, few NICUs have recognized theutility of having objective measures to help prevent,diagnose, and treat milk volume problems.(5)(6)(7)(10)(11) In our Rush Mothers’ Milk Club™program, mothers of NICU infants maintain profession-ally produced milk volume records (Figure) that serve asa breastfeeding memento for pump-dependent women.(10)(11)(12)(22)(23) Information from the mother-maintained records is transferred into a hand-held com-puter that subsequently downloads into the electronicmedical record for each infant on a weekly basis. Thus,the bedside clinicians can monitor the average daily milkvolume and number of pumpings constantly for eachmother to ensure that the infant receives the maximumamount of FHM.

To prevent insufficient milk volume later in the NICUstay, the Rush Mothers’ Milk Club educates women thata desirable milk volume target is at least 350 mL/d by theend of the second postnatal week. This figure is based onthe VLBW or ELBW infant requiring this volume atNICU discharge if the mother wants to feed her milk

exclusively. Higher volumes (500 to 1,000 mL/d) areeven more desirable because they ensure “extra milk”during the inevitable times of stress-induced lactationproblems during the infant’s NICU stay. In addition, theextra milk produced during the first weeks can be frozenfor later use during and after the NICU stay. In the RushMothers’ Milk Club, all extra milk is kept onsite inindustrial freezers that have computerized temperaturecontrol alarms, so it can be fed as needed. The onsitestorage ensures that the milk is safely cared for andremoves the barrier of inadequate home freezer storagefor low-income women, who otherwise would have todiscard extra milk or downregulate milk production.

Troubleshooting Common Milk VolumeProblems in Pump-dependent WomenSignificantly more research has been conducted on thephysiology of lactation for breastfeeding mothers ofhealthy infants than for pump-dependent women.(24)(25)(26)(27)(28)(29)(30)(31) Studies of breast-feeding mothers underscore the importance of the inter-play between the endocrine and autocrine control of milksynthesis, which translates clinically into frequent andcomplete milk removal to avoid the downregulation of

Table. Best Practices (continued)

• A mother who has previously produced an adequate volume of milk is more likely to respond favorably than amother who has primary insufficient milk volume

• Review maternal risk factors and the use of other medications to determine if metoclopramide is an appropriateoption

• If metoclopramide is an appropriate option, provide the mother with the educational tear sheet, explaining the useof the medication as a galactagogue–The tear sheet details the indications, dosing, and potential untoward effects of metoclopramide–Explain to the mother that the prescribing clinician may not know of the use of metoclopramide as agalactagogue because it is a specialty within lactation management

–Provide mother with pager number so that prescribing clinician can speak with the NICU lactation specialist ifmore information about metoclopramide is required

–Instruct the mother to use the toll-free lactation pager to communicate with the NICU lactation specialist on day2 of metoclopramide therapy and any time that an untoward effect may be suspected

• Instruct the mother to maintain milk volume records during metoclopramide therapy• Note that the mother is receiving metoclopramide therapy in the infant’s medical record

3. Consider whether the mother would benefit from short-term prescription antianxiety or sleep aids.• Mothers who are especially likely to benefit from these medications are those who have newly admitted NICU

infants or those who have experienced a clinical setback and report anxiety and inability to sleep due to concernsabout the infant

• Emphasize to the mother that these medications are not “long-term” antidepressant or antianxiety medications, butprovide short-term symptom relief to make the NICU setting more manageable

• Recommend specific medications to the mother that are compatible with lactation• Offer to communicate with the mother’s primary clinician to discuss these medications and assure the clinician of

their appropriate use during lactation4. Encourage the mother to attend the weekly Mothers’ Milk Club luncheon meetings so that she receives peer support

for her lactation efforts.




these processes during prolonged storage of milk in thebreast. (27)(29)(31)(32)(33) Simply stated, milk re-maining in the breast due to an ineffective breast pump,a tightly fitted breast shield, or infrequent pump usepredisposes mothers to low milk volume within a fewdays through the feedback inhibitor of lactation mecha-

nism. (33) Clinically, it is not un-common for a pump-dependentwoman producing 700 mL/d tolose 50% of her milk volume within2 to 3 days after changing from aneffective hospital-grade pump to aless-effective manual pump or withdecreasing her pumping from 8 to4 times daily.

Another common reason for arapid decline in milk volume inmothers of infants in the NICU isthe early administration ofprogestin-based hormonal birthcontrol, sometimes prior to themother’s discharge from the hospi-tal after giving birth. (10)(14)Whereas progestin-based birthcontrol is unlikely to affect estab-lished lactation with a healthybreastfed infant, such findings can-not be applied indiscriminately tothe pump-dependent mother whostill is establishing an adequate milkvolume in the first weeks after birth.(10)(14)(34) The physiologicmechanism is as follows. Prior todelivery, progesterone suppressesthe milk synthesis role of prolactin,which is present in high concentra-tions during the late antenatal pe-riod. (21)(31)(34) Following de-livery of the placenta, theprogesterone concentration de-clines dramatically and coincideswith the onset of lactogenesis II orthe change from small to copiousamounts of milk. (14)(21)(31)When progestin-based birth con-trol methods are introduced dur-ing this vulnerable transition,milk synthesis can be inhibitedsignificantly, in a manner similarto that documented for a retainedplacenta. (14)(35) Thus, it is im-

portant that mothers receive information about alter-native contraceptive options that are used more appro-priately during early lactation.

Finally, many mothers of VLBW and ELBW infantsexperience delayed lactogenesis or the milk “coming in”after the third postnatal day. (10)(13)(14)(15)(16) Al-

Figure. My Mom Pumps for Me!TM Maternal Milk Volume Record.® The 5�7-inch milkvolume record serves as a breastfeeding momento for pump-dependent mothers of NICUinfants. The hard cover opens to reveal a checkbook type insert (1 page for 1 day) onwhich the mother records the milk volume and number of minutes for each daily pumpingand then totals these figures for a 24-hour period. This summary information is recordedin hand-held computers by the NICU lactation team and downloaded into the infant’smedical record. The pocket above the checkbook insert contains a card for the infant’sisolette. Once the card is removed, the pocket holds a photograph of the infant that themother can see when pumping away from the infant’s bedside.




though delayed lactogenesis has not been studied thor-oughly, several risk factors have been proposed and in-clude preterm labor, pregnancy-induced hypertension,blood loss, prolonged bed rest, cesarean delivery, andmedications to manage many of these problems.(13)(14)(15)(16)(17)(18) Clinically, delayed lactogen-esis presents as a mother being able to provide only dropsof milk, despite using a breast pump for 15 minutesseveral times daily. The evidence suggests that, unlessaccompanied by other primary lactation problems, de-layed lactogenesis is temporary, with the affected moth-ers eventually producing comparable volumes of milk asunaffected mothers. (13)(14)(17)(18) However, moth-ers can become discouraged during these early daysunless they receive evidence-based information about thetemporary nature of delayed lactogenesis. Additionally,they must be encouraged to use the breast pump tostimulate the breasts, even though little milk is removed.Manual expression used in combination with pumpingmay be most effective in removing available milk duringthese early days.

Mothers also can be reassured that the relatively smallvolumes of milk during the early days of pumping aremore medicinal than nutritive, based on findings froma small body of studies about the composition of“preterm” colostrum. (36)(37)(38)(39) Colostrum,the milk that is produced during the first postnatal days,is a function of open paracellular pathways in the mam-mary epithelium that permit the “leaking” of variousmaternal components into the milk. (21)(37) The evi-dence suggests that these open paracellular pathwaysresult in greater absolute concentrations of protectivesubstances than for a term birth and that the tightjunctions close more gradually. (36)(37)(38)(39) Thus,the relatively small volumes of colostrum that accompanydelayed lactogenesis may be physiologically importantfor VLBW and ELBW infants, who benefit from theprolonged anti-infective, anti-inflammatory, and growthfactor components in preterm colostrum. This informa-tion is especially motivating for mothers who may be-come discouraged with producing only drops of co-lostrum for the first few days after birth.

Management of Insufficient Maternal MilkVolume in Pump-dependent WomenIn most instances, insufficient maternal milk volume inpump-dependent women is a function of prolonged milkstasis or intense anxiety that can be managed nonphar-macologically by ensuring that interventions in the Tablehave been implemented. However, galactagogues andshort-term antianxiety or sleep medications also can be

used to treat insufficient maternal milk volume in se-lected instances.

Domperidone and metoclopramide are commonlyused off-label as galactagogues, and several studies havedemonstrated their effectiveness in increasing baselineprolactin concentrations and mean daily maternal milkvolume. (40)(41)(42)(43)(44) However, domperidone,which does not cross the blood-brain barrier and is usedwidely in Canada and Europe, is not approved for use bythe United States Food and Drug Administration. Thesemedications do not affect the suckling-induced prolactinsurge that occurs only following sucking (or pumping)and breast emptying, so they are ineffective if the motherdoes not continue frequent breast pump use. (32)(40)(41)(42)(43)(44) Although these medications typicallyare used short-term, there are no data to indicate that amother who responds well to them cannot continue theiruse as long as she remains free of untoward effects. In theRush Mothers’ Milk Club Program, we do not routinelydiscontinue metoclopramide in women for whom it iseffective in the absence of untoward effects. Our experi-ences with many women over the past 10 years suggestthat maintenance doses of 30 mg can be tolerated wellfor several weeks. Similarly, once the milk volume hasbeen re-established for 2 to 3 weeks, some pump-dependent mothers can sustain that same milk volumewhile receiving 20 mg daily in combination with fre-quent breast pump use.

Finally, although many herbal and dietary supple-ments are recommended as alternatives to prescriptionmedications for treatment of insufficient milk volume,these products have not been studied systematically. (14)Many clinicians make the mistake of trying an herbalremedy for several days prior to initiating prescriptiongalactagogues, only to see the baseline maternal milkvolume decline even further, rendering the prescriptionagents less effective in doubling baseline volumes.Herbal remedies may be used best for mothers who arenot candidates for prescription agents or for those forwhom the objective is preventing rather than treatinginsufficient milk volume.

Nearly all mothers of NICU infants experience in-tense stress, anxiety, and difficulty sleeping during thefirst days or weeks after birth, when their infants are themost critically ill. (10)(19)(20) Such emotional re-sponses can have a negative effect on maternal milkvolume through triggering of the dopaminergicprolactin-inhibiting factor or through inhibition of theoxytocin-mediated milk ejection reflex. (19)(20)(32)(41)(45) Although nonpharmacologic strategiessuch as unrestricted 24-hour visitation policies, skin-to-




skin holding, and suckling at the emptied breast may beeffective, (10)(11)(12)(46) clinicians also should con-sider the use of short-term antianxiety and sleep medica-tions during the time that the symptoms are most acute.No systematic study has examined the effect of suchmedications on maternal milk volume, but they are ef-fective in promoting rest and managing anxiety and canbe used safely on a temporary basis during lactation.(40)(41)

In summary, the evidence suggests that insufficientmilk volume occurs more frequently than necessary inpump-dependent mothers of VLBW and ELBW infants,with the effect of reducing the amount of FHM that suchinfants receive. Allocation of NICU resources that prior-itize the prevention, diagnosis, and treatment of insuffi-cient milk volume for mothers of these infants, using thepractices outlined in the Table, could reduce the overallprevalence of this problem.

Management of Slow Weight Gain forFHM-fed VLBW and ELBW InfantsIt is well-recognized that ELBW and VLBW infants maynot gain weight as rapidly when receiving FHM as whenreceiving commercial formula during the first postnatalweeks, especially if the infants are volume-restricted dueto other clinical complications. (1)(2)(9) Typically, slowweight gain results in the substitution of calorie-densecommercial formulas for some daily feedings, reducingthe exclusive use of FHM in this population.

Although the research literature has documentedconsistently that storage and handling procedures canreduce available milk lipid and that there is significantvariability in caloric content in expressed human milk fedin the NICU, most clinicians still erroneously assumethat all human milk contains 20 kcal/oz. (47)(48)(49)(50)(51)(52) Research technologies used in studiesof human milk, such as the creamatocrit procedure, areespecially applicable in managing slow weight gain forVLBW and ELBW infants because they permit an accu-rate diagnosis for the slow weight gain.

Utility of the Creamatocrit to Manage FHMFeedings in the NICU

The creamatocrit technique, first described in 1964 (53)and subsequently validated for human milk in 1978, (54)is a quick, accurate, easy-to-perform, and inexpensiveprocedure for estimating the lipid and caloric content inhuman milk. (48)(49)(50)(54)(55) The creamatocrit isthe research technique of choice for human milk scien-tists who do not have access to direct laboratory measures

of milk components, and it has been used in innumerableresearch investigations. (49)(56) Performed like the he-matocrit, the creamatocrit involves placing human milkin capillary tubes and spinning the tubes in a hematocritcentrifuge, which separates the cream layer from theaqueous phase of the milk. The cream layer and totalvolume are measured, and the creamatocrit is calculatedas the percent of total volume represented by cream. Thispercentage is converted to lipid and caloric content usingregression algorithms from the research literature.(47)(48)(49)(50)(54)(55)(56)

In the past, creamatocrit measures could be per-formed only with a standard laboratory centrifuge andcalipers or a hematocrit reader, which limits the feasibilityof the technique in the NICU. (48)(49)(50)(51) How-ever, a small, portable, noiseless centrifuge specificallydesigned for measuring the creamatocrit that spins in3 minutes is ideal for use in the clinical setting and can beused to diagnose and manage slow weight gain for FHM-fed infants. (49) The device has an embedded reader thateliminates the need for calipers or a hematocrit readerand that electronically calculates calorie (kcal/oz andkcal/L) and lipid (g/L) content from the creamatocritvalue. A blinded trial has demonstrated the accuracy andprecision of the device with milk samples that ranged incalorie and lipid content from lows of 506.02 kcal/L and18.3 g/L to highs of 1,452.62 kcal/L to 119.4 g/L,respectively. (49) Thus, this instrument can be used inthe clinical setting with the confidence that it has beenstudied with a population of pump-dependent mothersof NICU infants who provided heterogeneous milk sam-ples.

Using the Creamatocrit to Diagnose andManage Slow Weight Gain in the NICU

When combined with a basic understanding of the prin-ciples of lactation science, the creamatocrit is an invalu-able tool for diagnosing and managing slow weight gainin FHM-fed VLBW and ELBW infants. First, creamat-ocrit values differentiate whether slow weight gain is afunction of low lipid and calories in the individuallycollected milk specimens or whether it results from lipidlosses that occur during storage, handling, and feeding ofthe milk. Creamatocrit measures can be used to managethe diagnosed problem, eg, a mother’s milk that is nat-urally low in calories or an infant who requires slow-infusion gavage feeding during which lipid adheres to theinfusion tubing.




Variability in Lipid and Calorie Content inIndividually Collected Milk SamplesVARIABILITY WITHIN A SINGLE PUMPING. Unlike

commercial formula, the lipid (and thus, the caloric)content of human milk varies significantly, with severalfactors particularly affecting pump-dependent women.(48)(49)(56)(57) First, the lipid globules in human milkare not released from the mammary epithelium in aconstant manner during breast emptying; instead, theyare secreted into the milk following the milk ejectionreflex and increase as a percentage of milk volume overthe remaining minutes of pumping. (28)(30)(31)(56)(57) Thus, foremilk that is removed in the first fewminutes is typically low-lipid and low-calorie, whereashindmilk that is removed in the last few minutes is lipid-and calorie-rich. (58) Accordingly, a mother who stopspumping prior to complete emptying of the breasts, asoften happens when all mothers are given the sameguideline for pumping duration, inadvertently may col-lect low-calorie milk for her infant because the higher-lipid milk remains in the breasts. Similarly, a mother whohas a large milk volume and expresses directly into 2-ozmilk storage containers may unknowingly separate theforemilk and hindmilk because all of her milk does not fitinto a single storage container. If her 600-g infant is fedthe low-calorie foremilk for several sequential days,weight gain will be slow. Both of these problems arepreventable.

VARIABILITY BETWEEN MOTHERS. Second, there issignificant between-mother variability in caloric and lipidcontent in human milk, which is not a problem for theterm healthy infant who simply consumes a greater vol-ume of milk when a mother has lower milk lipid content.(48)(49)(50)(51)(59) However, for the mother whoseinfant in the NICU cannot consume a larger volume,low-lipid milk can be a problem. The between-mothervariability in caloric and lipid content in human milk washighlighted in a recent study in which 12 mothers ofNICU infants provided specimens of foremilk, hindmilk,and composite milk (milk from a complete pumping orbreast emptying) during the same pumping session for atotal of 36 milk specimens. Whereas the mean caloric andlipid content in the composite milk specimens were26.2 cal/oz and 56.4 g/L, respectively, these valuesvaried from a low of 18.1 cal/oz and 29.1 g/L to a highof 33.9 cal/oz and 85.3 g/L. (49) In multiple instances,some mothers’ composite or foremilk specimens had ahigher caloric and lipid content than other mothers’hindmilk specimens. Clinically, a mother who naturallyproduces lower-lipid milk can be taught to provide hind-

milk, which involves separating the lower-lipid foremilkfrom the remainder of the expressed milk during pump-ing. (47)(58) A target caloric content in the hindmilk canbe validated by the creamatocrit procedure and fed to theinfant, whereas the foremilk can be frozen for later use.

VARIABILITY WITHIN MOTHERS. Finally, lower-lipidmilk also is a function of prolonged milk storage in thebreast, as occurs naturally when pumping intervals arewidely spaced. (29)(31) Although this is not a problemfor the mother who has a healthy breastfeeding infantwho feeds on demand throughout the day, it is a com-mon clinical scenario for the pump-dependent motherwho sleeps long stretches at night and removes thegreatest volume of milk during the first pumping of themorning. This early-morning milk usually is the lowestcalorie of the day, but because it represents the greatestsingle pumped volume of the day, often it is sufficient fora 24-hour feeding volume for the VLBW or ELBWinfant. A clinical example from the Rush Mothers’ MilkClub program illustrates the consequences of this com-mon clinical scenario.

An infant born at 24 weeks’ gestation who had gainedadequate weight on exclusive mother’s milk feedingsdemonstrated an average daily weight gain of only 5 g for1 week at 30 weeks of gestation. The mother’s milkvolume records documented that she pumped six timesdaily for an average daily milk volume of 800 mL, but shedid not pump for an 8-hour interval during the night. Onawaking, she pumped nearly 300 mL of milk, represent-ing 38% of the daily milk volume, in a single milkexpression. She placed most of this milk into a single240-mL storage container. During the remainder of theday, she pumped every 2 to 3 hours and removed 100 to120 mL of milk, which she placed into 120-mL storagecontainers. The bedside nurse noted that the larger stor-age container provided a 24-hour volume for the 30-week-old infant and chose to feed this early morning milkand freeze the later-in-the-day pumpings for later use.

Clinicians suspected that the slow weight gain re-flected the exclusive feeding of low-lipid, early-morningmilk, a theory that was validated with a creamatocritmeasure revealing a caloric content of 17 kcal/oz. Crea-matocrits performed on milk pumped later in the daywith shorter milk storage intervals were 27 to 31 kcal/oz. The problem was managed by freezing the early-morning pumped milk and feeding the milk collectedduring the day following shorter storage intervals. In theensuing week, the mean daily weight gain for the infantwas 22 g.




Storage, Handling, and Feeding ProceduresReduce Baseline Lipid in Human Milk

Separate studies of the handling and feeding of humanmilk demonstrate that the human milk lipid, which is nothomogenized, readily adheres to all types of plastic sur-faces, reducing the caloric content in milk that is fed tothe infant. (60)(61)(62) Adherence of lipid to the crev-ices of milk storage containers or the gavage infusiontubing can result in the infant receiving low-calorie milk,despite adequate baseline lipid and calories. Evidence-based procedures to ensure that stored human milk ismixed thoroughly, that fat does not remain in the storagecap or hard-to-reach areas in the container, and thatgavage infusion is over the shortest possible time areimportant troubleshooting tasks.

The creamatocrit procedure can be used to detectwhere the lipid losses occur in the processes of storing,handling, and feeding. For example, studies have dem-onstrated a significant decrease in lipid and calories dur-ing continuous gavage infusion of human milk, with aninverse relationship between caloric loss and infusionrate. (60)(61)(62) The research design for these studiesinvolved comparing the preinfusion and postinfusionlipid and calories in the human milk specimen, using asimulated feeding model. The NICU clinician can per-form this same comparison for an individual infant todetermine the magnitude of lipid and calorie loss duringgavage feedings by using the creamatocrit procedure.Either the rate of the feeding can be increased to mini-mize lipid and calorie loss or the mother can be asked toprovide hindmilk to compensate for the losses duringslow infusions of FHM. The creamatocrit can be used tohelp the mother achieve a desirable baseline caloric con-tent that compensates for the infusion-related lipidlosses.

NICU Mothers Can Perform CreamatocritsThe Rush Mothers’ Milk Club program completed atwo-phase blinded trial to determine whether mothers ofNICU infants could be taught to perform creamatocritsaccurately on their own milk specimens, using the stan-dard laboratory centrifuge and a hematocrit reader. (63)Findings revealed that the mothers performed these mea-sures as accurately as advance practice nurses, that theyfelt comfortable performing the measures, and that theysaved 186 minutes of nursing time over a 14-day periodby measuring a creamatocrit each day. These data re-vealed an inverse relationship between accuracy of crea-matocrit measures and the mothers’ reported householdincome, indicating that lower-income women tended toperform creamatocrits with greatest accuracy. Similarly,

mothers who had fewer than 10 years of formal educa-tion performed creamatocrits significantly more accu-rately than mothers who had greater than 16 years offormal education. Thus, our findings suggest thatwomen from all backgrounds can perform creamatocritsaccurately on their own milk.

SummarySeveral recent studies suggest a dose-response relation-ship between the amount of FHM received by VLBWand ELBW infants and protection from prematurity-specific morbidities. NICU clinicians must prioritize theprevention, diagnosis, and management of insufficientmaternal milk volume and slow infant weight gain toprovide these infants with the highest possible dose ofFHM over the NICU stay. Techniques from the humanmilk science field, particularly the use of maternal milkvolume records and the creamatocrit procedure, haveenormous potential for managing these common NICUproblems and are ideally suited to the NICU environ-ment.

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NeoReviews Quiz

4. Mothers of preterm infants often experience delays in the initiation of lactation and produce less milk thantheir term counterparts. Of the following, the most commonly assumed incorrect reason cited by cliniciansto explain such lactation complications is:

A. Insufficient monitoring of daily milk volumes.B. Lack of information and equipment for lactation.C. Lack of on-site milk storage.D. Maternal stress of neonatal intensive care.E. Preterm gestation.

5. Of the following, the most common reason for the decline in an established milk supply in pump-dependent mothers of preterm infants is:

A. Complication of cesarean delivery.B. Initiation of progestin-based contraception.C. Milk stasis due to incomplete emptying of breasts.D. Prolonged bed rest.E. Unresolved pregnancy-induced hypertension.

6. The creamatocrit technique is a quick, accurate, easy-to-perform, and inexpensive procedure that can beused for diagnosing and managing slow weight gain in fortified human milk-fed infants. Of the followingfactors in human milk, the technique is most accurate in measuring the content of:

A. Vitamin D.B. Lipids.C. Lactose.D. Iron.E. Carbohydrate.




DOI: 10.1542/neo.8-11-e467 2007;8;e467-e477 NeoReviews

Paula P. Meier and Janet L. Engstrom Low-birthweight Infants

Evidence-based Practices to Promote Exclusive Feeding of Human Milk in Very

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evidence-based practices to promote exclusive feeding of human milk in vlbw infants

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